Download Some Analogies Between Visual Cortical and Genetic Maps

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Chapter 16
Maps in Context: Some
Analogies Between Visual
Cortical and Genetic Maps
John Allman
16.1
Introduction
The purpose of this essay is to examine some parallels in the evolutionary
and functional significance of replicated maps in the genetic material and
the visual cortex. In particular, I would like to explore two related ideas.
The first is that the differentiation of replicated maps is an important factor
in the development of new functional capacities in evolution. The second is
that the properties of maps are influenced by their context. The contextual
influences are mediated in genetic systems by various forms of gene regula­
tion. In the visual cortex, contextual influences are expressed by the effects
of stimuli located outside the classical receptive fields of individual neurons
making up each cortical map. These contextual influences may determine
how the organs of the body are assembled by the genes and how percepts
369
L. M. Vaina (ed.), Mallers of ]ntelligence, 369-393.
© ]987 by D. Reidel Publishing Company.
JOHN ALLMAN
370
and thoughts emerge from the activity of mapped arrays of neurons.
16.2
Multiple maps in the genetic material
The first successful mapping of the genetic material was accomplished by
Morgan! in 1911 when he deduced that substances controlling certain sex­
linked traits, such as eye-color, were located in the X-chromosome in the
fruit fly, Drosophilia. The presence in the salivary glands of giant chro­
mosomes, 100 times the size of chromosomes in other cells, enormously
facilitated gene mapping in fruit flies. The microscopic examination of the
salivary gland chromosomes revealed a detailed pattern of transverse bands
of different thickness and structure. Bridges 2 noted that these patterns fre­
quently were duplicated in different parts of the chromosomes. He later
remarked:
"In my first report on duplications at the 1918 meeting of the
A.A.A.S., I emphasized the point that the main interest in du­
plications lay in their offering a method for evolutionary increase
in lengths of chromosomes with identical genes which could sub­
sequently mutate separately and diversify their effects."g
It is ironic that Bridges waited 17 years to publish this revolution­
ary idea which has become central to the study of the molecular basis
of evolution. 4 Lewis 5 and Ohno 6 extended this concept by pointing out
that duplicated genes escape the pressures of natural selection operating
on the original gene and thereby can accumulate mutations which enable
1 T. H. Morgan, "An attempt to analyze the constitution of chromosomes on the basis
of sex-limited inheritance in drosophilia," J. Experimental Zoology, 11, 365-413, 1911.
2C. B. Bridges, "Salivary chromosomes maps," J. He reddy, 26,60-64, 1935.
3 ibid, page 64.
4 "Gene duplication is probably the most important mechanism for generating new genes
and new biochemical processes that have facilitated the evolution of complex organisms
from primitive ones." W.-H. Li, "Evolution of duplicate genes and pseudogenes," in:
Evolution of Genes and Proteins, Masatoshi Nei and Richard K. Koehn, eds., Sinauer
Assoc., Sunderland, Mass., 1983, page 14.
5E. B. Lewis, "Pseudoallelism and gene evolution," Cold Spring Harbor Symposia on
Quantitative Biology, 16, 159-174, 1951.
uS. Ohno, Evolution by Gene Duplication, Springer-Verlag, New York, 1970.
t
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MAPS IN CONTEXT: VISUAL CORTICAL AND GENETIC MAPS
[
371
the new gene to perform previously non-existent functions, while the old
gene continues to perform its original and presumably vital functions. One
of the earliest and most elegant examples of the role of gene duplication in
evolution was discovered by Ingram,7 who compared the structure of the
oxygen carrying proteins myoglobin, a monomere, and its tetrameric rela­
tive, hemoglobin. He deduced that at an early stage in vertebrate evolution,
the heme protein inside muscle cells was the same as that in the circulation.
The muscle heme protein became myoglobin in the course of evolution; it
retained a molecular weight of 17,000 and only one heme group and one
peptide chain per molecule. However, the gene producing the circulating
heme protein duplicated several times to produce the structure of modern
hemoglobin with four homologous peptide chains. Another example is the
vast number of closely related immunoglobin genes. s Finally, Britten and
Kohne 9 developed a technique for determining the abundance of replicated
DNA sequences for the entire genomes of higher organisms. They separated
the complementary stranQsof the DNA and sheared them into fragments of
about 400 nucleotides in length. Then they measured the time required for
the complementary strands to reassociate at different concentrations. They
found that much of the DNA reassociated far more rapidly and at lower
concentrations than would be expected if there were no redundancy in the
DNA sequence, which led to their estimate that more than one-third of
the DN A in higher organisms is made up of sequences which are replicated
many times. They concluded:
"The families of repeated sequences range from groups of
almost identical copies to groups with sufficient diveI:sity that,
after reassociation, only structures of low stability are formed
among the members. It seems likely that this situation has
arisen from large-scale precise duplication of selected sequences
with subsequent divergence caused by mutation and the translo­
7V. M. Ingram, The Hemoglobins in Genetics and Evolution, Columbia University
Press, New York, 1963.
sL. Hood, J. H. Campbell and S. C. R. Elgin, "The organization, expression and
evolution of antibody genes and other multigene families," Ann. Review of Genetics, 9,
305.353, 1975.
gR. J. Britten and D. E. Kohne, "Repeated sequences in DNA," Science, 161,529·540,
1968.
JOHN ALLMAN
372
cation of segments/HO
They further suggested that each family of repeated sequences arose
from relatively sudden events in evolutionary history, which they called
"saltatory replications."
16.3
MUltiple maps in the visual cortex
In contrast to the linear maps of amino-acid sequences in the base code
sequences of the DNA, the representations of the visual field in the vi­
sual cortex are two-dimensional. The mapping of the visual cortex began
earlier, but has proceeded more slowly than the mapping of the genetic
material. In 1881, Munk 11 located the visual cortex in the occipital lobe
by making a series of selective lesions in macaque monkeys and observing
their post-operative deficits in behavior. After this promising beginning,
however, it was not for another generation that the representation of the
visual field in the primary visual cortex was established by Inouye 12 and
Holmes 13 who related visual field defects to the sites of visual cortex lesions
in soldiers who had been injured in the Russo-Japanese and First World
Wars respectively. The development of amplifiers and oscilloscopes made
possible the electro-physiological study of the responses of the visual cortex
beginning in the 1940's. By recording visually evoked potentials, Talbot
14 and Marshall, Talbot and Ades 15 found evidence for several areas be­
yond the primary visual cortex in cats. The development of microelectrode
lOibid, page 39.
Munk, Uber die Funktionen der Grosshirnrinde, A Hirnwald, Berlin, 1881. English
translation in G. Von Bonin, Some Papers on the Cerebral Cortex, pp. 97-117, Thomas,
Springfield, Illinois, 1960.
12T. Inouye, Die Sehstorungen bei Schussverletzungen der Kortialen Sehsphare, nach
Beobachtungen an Verwundeten der letzten Japanischen Kriege, W. Engelmann, Leipzig,
1909.
13G. M. Holmes, "Disturbances of vision by cerebral lesions," Brit. J. Ophthalmology,
2, 353, 1918.
14S. A. Talbot, "A lateral localization in the eat's visual cortex," Federfltion Proc., 1,
84, 1942.
V..,W. H. Marshall, S. A. Talbot and H. W. Ades, "Cortical response of the anesthetized
cat to gross photic and electrical afferent stimulation," J. Neurophysiology, 6, 1-15, 1943.
11 H.
MAPS IN CONTEXT: VISUAL CORTICAL AND GENETIC MAPS
373
recording 16 from single neurons enabled Hubel and WiseP7 to conduct their
landmark study of the functional organization of two higher cortical visual
areas in cats. Inspired by their work, Jon Kaas and I began in 1968 to map
the representations of the visual field in the non-primary or extra-striate
visual cortex in primates. These regions were presumed to perform higher
functions in the analysis of visual information, since the anatomical con­
nectional studies by Polyak 18 indicated that the visual input was mainly
funneled through the primary or striate visual·cortex. We chose to map the
visual cortex in owl monkeys because they possessed a relatively smooth
cerebral cortex unencumbered by the deep fissures found in most species of
simian primates. We found a virtual embarrassment of riches in the visual
cortex of the owl monkey, for instead of there being three or four maps of
the visual field as we expected, we soon found evidence for about 10 visual
areas which comprised the posterior third of the cortex. (See Figures 16.1
and 16.2.) At the time we were blissfully ignorant of the developments in
modern 'genetics described in the first section, but we were aware of the
idea advanced many years earlier by the paleontologist Gregory 19 that
a common mechanism of evolution appears to be the replication of body
parts due to a genetic mutation in a single generation followed in subse­
quent generations by the gradual divergence of structure and functions of
the replicated parts. 20 We suggested this mechanism as an alternative to
the view that topographically organized sensory representations gradually
differentiated from "unorganized" cortex, or that individual topographi­
cally organized areas gradually differentiated into additional topographical
representations.
The evidence for multiple maps in cerebral cortex has cascaded. Work­
ing at the 'same time, and for a period in the late 1960's at the same place
U'D. H. Hubel, "Tungsten microelectrode for recording from single units," Science, 125,
549-550, 1957.
17D. H. Hubel and T. N. Wiesel, "Receptive fields and functional architecture in two
non-striate visual areas (18 and 19) of the cat," J. Neurophysiology, 28, 229-289, 1965.
18S. Polyak, Th.e Main Afferent Fiber Systems of th.e Cerebral Cortex in Primates, Uni­
versity of California Press, Berkeley, 1932.
lDW. K. Gregory, "Reduplication in evolution," Quarterly Rev. of Biology, 10,212-290,
1935.
20 J. M. Allman and J. K. Kaas, "A representation of the visual field in the ca.udal third
of the middle tempora.l gyrus of the owl monkey (Aotus trivirgatus)", Brain Res., 31,
85-105, 1971.
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JOHN ALLMAN
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JOHN ALLMAN
(the University of Wisconsin), Zeki 21 uncovered evidence for a number of
cortical visual areas in macaque monkeys. Spatz and Tigges,22 Gross and
colleagues,23 Desimone and Ungerleider,24 and Maunsell and Van Essen 25
have also made major discoveries in the simian extrastriate cortex.
Rosenquist, Palmer and Tusa26 have mapped in cats an extensive ar­
ray of visual areas, many of which have probably arisen independently in
evolution from those in primates.
There is fossil evidence that visual cortex underwent rapid expansion
in the early primates. (See Figure 16.3.) The primitive mammals that
were the common ancestors of the living eutherian mammals had poorly
developed visual systems, and depended instead on olfaction, touch and
hearing. 27 However, primates, which emerged as a very successful group
rather suddenly at the beginning of the Eocene, 55 million years ago, pos­
sessed large frontally directed eyes and a greatly expanded visual cortex. 28
This suggests that the large array of extrastriate visual areas in primates,
like some of the families of repeated DNA sequences, may have arisen during
21S. M. Zeki, "Functional specialization in the visual cortex of rhesus monkey," Nature,
274,423-428, 1978. References 22 through 26 list some of the major publications on the
topographic organization of the cortical visual areas.
22W. B. Spatz and J. Tigges, "Experimental-anatomical studies on the 'Middle Temporal
Visual Area (MT)' in primates. 1. Efferent corticocortical connections in the marmoset
(Callithrix jacchus)" , J. Comparative Neurology, 146, 451-463, 1972.
23C. Gross, C. Bruce, R. Desimone, J. Fleming and R. Gattass, "Cprtical visual areas
of the temporal lobe," in: Multiple Cortical Visual Areas, pp. 187-216, C. N. Woolsey, ed.,
Humana Press, Clifton, New Jersey, 1981.
24R. Desimone and L. Ungerleider, "Multiple visual areas in the caudal superior tem­
poral sulcus of the macaque," J. Comparative Neurology, in press.
25 J. H. R. Maunsell and D. C. Van Essen, "The connections of the middle temporal
visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey,"
J. Neuroscience, 3, 2563-2586, 1983.
2GR. J. Tusa, L. A. Palmer and A. C. Rosenquist, "Multiple cortical visual areas: visual
field topography in the cat," in: Multiple Cortical Visual Areas, pp. 1-31, C. N. Woolsey,
ed., Humana Press, Englewood Cliffs, New Jersey, 1981.
27M. Cartmill, "Rethinking primate origins," Science, 184, 436-443, 1974.
8
2 L. B. Radinsky, "The oldest primate elldocast," American J. Physical Anthropology,
27, 385-388, 1967. L. B. Radinsky, The Fossil Record of Primate Brain Evolu.tion, Amer­
ican Museum, New York, 1979. J. M. Allman, "The evolution of the visual system in
the early primates," in: Progress of Psychobiology and Physiological Psychology, James
Sprague and Alan Epstein, eds., 7, I-53, Academic, New York, 1977.
MAPS IN CONTEXT: VISUAL CORTICAL AND GENETIC MAPS
relatively short periods of time in saltatory replications.
16.4
377
29
Maps and functions
One of the central ideas of modern genetics is that a particular gene contains
the instructions to make a particular protein that has a specific function.
One example is the system of genes for photoreceptor proteins. Recently,
Nathans et aj30 have mapped the DNA sequences of the genes for the rod
and cone receptor proteins in man. It appears on the basis of sequence
homologies that the genes that produce the rod and cone receptor proteins
are replicas of an ancient gene for a receptor protein. 31 The genes for the
red and green receptor proteins are located adjacent to each other on the X
chromosome and have a 96% sequence homology.32 Many individuals have
up to three slightly different versions of the gene for the green receptor
protein. It is not clear how these multiple green receptor genes contribute
to perception, but this result does point to a seeming redundancy in the
genetic organization of the visual system, which raises cOIJ:?parable questions
about the functional meaning of multiple cortical visual areas.
The notion that a cortical visual area performs a specific and probably
unique perceptual or information processing function has been the implicit
20"The first primates of modern aspect" appeared rather suddenly and in considerable
abundance at the beginning of the Eocene (Elwyn Simons, Primate Evolution, MacMillan,
New York, 1972). The ancestry of these Eocene primates is obscure. Most of the very
early primates, the plesiadapiformes, from the Cretaceous and Paleocene, appear to be too
specialized in their dentition and other features of their anatomy to have been ancestral
to later primates (F. S. Szalay and E. Delson, Evolutionary History of the Primates,
Academic, 1979). The brain case is small relative to skull size in the plesiadapiformes,
unlike the later primates.
30 J. Nathans, D. Thomas and D. Rogness, "Molecular genetics of human color vision:
the genes encoding blue, green and red pigments," Science, 232, 193-202, 1986.
31The receptor protein encoded by this ancient gene may not have been photoreceptive
in function, but had some other, perhaps more ubiquitous, receptor function.
32The comparative study of the photoreceptor genes could contribute much to our un­
derstanding evolutionary development of perceptual capacities. One approach would be
to study the system of the photoreceptor genes in New World Monkeys, which vary con­
siderably in their capacities to discriminate colors. (G. Jacobs, Comparative Color Vision,
Academic, New York, 1980.) It would also be very useful to determine how the central
mechanisms for color perception relate to organization of photoreceptor proteins in New
World Monkeys.
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MAPS IN GONTEXT: VISUAL CORTICAL AND GENETIC MAPS
379
or explicit hypothesis of most of the research conducted in the extrastriate
areas. However, perhaps the best evidence for this hypothesis comes not
from the visual cortex itself but from the dorsal lateral geniculate nucleus,
which receives input from the retina and relays to the visual cortex. In a
number of mammalian orders, including primates and carnivores that pos­
sess well developed visual systems with a fair degree of binocular vision,
the dorsal lateral geniculate nucleus is divided into a series of laminae re­
ceiving input from the ipsilateral or contralateral eye. 33 The laminae are
stacked in registers so that the same point in the visual field is represented
in a line approximately perpendicular to the laminae. Most carnivores
have two major laminae. Laminae A receives input from the contralat­
eral hemiretinaj laminae Al receives input from the ipsilateral hemiretina.
However, these laminae are duplicated in minks and ferrets,34 and the re­
sponse properties of the cells in these laminae are segregated so that one
set of the duplicated laminae have neurons with ON-center receptive fields
while the other half have OFF-center receptive fields. 35 The ON and the
OFF center cells are mingled together in the unduplicated laminae in other
carnivores. This segregation of ON and OFF laminae is also present in
the dorsal lateral geniculate nucleus in tree shrews36 and to a less complete
extent in macaque monkeys.37. There is evidence in the mink that ON-OFF
segregation is maintained at the next level of visual processing in layer 4 of
primary visual cortex. 38
In monkeys, there exist strong quantitative distinctions betw'een the
two major sets of laminae in the dorsal lateral geniculate nucleus that re­
33 J. H. Kaas, R. W. Guillery and J. M~ Allman, "Some principles of organization in the
dorsal lateral geniculate nucleus," Brain, Behavior and Evolution, 6, 253-299, 1972.
.
34K. J. Sanderson, "Lamination of the dorsal lateral geniculate nucleus in carnivores of
the weasel (Mustilidae), raccoon (Procyonidae) and Fox (Canidae) families," J. Compar­
ative Neurology, 15S, 239-266, 1974.
3&S. LeVay and S. K. McConnell, "ON and OFF layers in the lateral geniculate nucleus
of the mink," Nature, 300, 350-351, 1982; M. P. Stryker and K. R. Zahs, "ON and OFF
sublaminae in the lateral geniculate nucleus of the ferret," J. Neuroscience, 3, 1943-1951,
1983.
30 J. Conway and P. Schiller, "Laminar organization of the lateral geniculate body and
the striate cortex in the tree shrew (Tupaia glis)," J. Neuroscience, 4, 171-197,1984.
37p. Schiller and J. Malpeli, "Functional specificity of lateral geniculate nucleus laminae
of the rhesus monkey," J. Neurophysiology, 41, 788-797, 1978.
38S. K. McConnell and S. LeVay, "Segregation of ON- and OFF-center afferents in mink
visual cortex," Proc. National Academy of Science, 81, 1590-1593,1984.
380
JOHN ALLMAN
lay input to the primary visual cortex. The magnocellular laminae contain
large cells that are fast conducting and receive fast input from the retina;
the parvocellular laminae contain smaller cells that are slower conducting
and receive slower input from the retina. 39 The neurons of the magno­
cellular laminae are much more sensitive to low contrast stimuli and have
larger receptive fields. 4o The magnocellular laminae contain proportionally
smaller representations of the central visual field than do the parvocellular
laminae. 41 The neurons in the parvocellular laminae of macaque monkeys
are rich in opponent-color mechanisms. 42
The magnocellular laminae project to layer 4Ca of primary visual cortex
(V_I),43 then to the adjacent layer 4B44, then to the middle temporal vi­
sual area (MT).45 The neurons in layer 4B of V_I46 and in MT47 are usually
39S. M. Sherman. J. R. Wilson, J. H. Kaas and S. V. Webb. "X- and V-cells in the dorsal
lateral geniculate nucleus of the owl monkey {Aotus trivirgatus)," Science. 192. 475-477,
1976; B. Dreher, Y. Fukada and R. W. Rodieck, "Identification, classification and anatom­
ical segregation of cells with X-like and V-like properties in the lateral geniculate nucleus
of old-world primates," J. Physiology. 258. 433-452, 1976; P. Schiller and J. Malpeli, opus
cit., 1978.
4°E. Kaplan and R. M. Shapley, "X and Y cells in the lateral geniculate nucleus of
macaque monkeys," J. Physiology, 330, 125-143, 1982; A. M. Derrington and P. Lennie,
"Spatial and temporal contrast sensitivites of neurons in lateral geniculate nucleus of
macaque," J. Physiology, 351, 219-240, 1984.
41 M. Connolly and D. Van Essen, "The representation of the visual field in the parvocel­
lular and magnocellular laminae of the lateral geniculate nucleus in the macaque monkey,"
J. Comparative Neurology, 226, 544-564, 1984.
42T. N. Wiesel and D. H. Hubel, "Spatial and chromatic interactions in the lateral
geniculate body of the rhesus monkey," J. Neurophysiology, 29, 1115-1156, 1966.
<l3D. H. Hubel and T. N. Wiesel, "Laminar and columnar distribution of geniculo-cortical
fibers in the macaque monkey," J. Comparative Ne'urology, 146, 421-450, 1972.
44 J. Lund, "Organization of neurons in the visual cortex Area 17 of the monkey {Macaca
mulatta)," J. Comparative. Neurol., 147,455-496, 1973.
4&W. B. Spatz, "Topographically organized reciprocal connections between areas 17 and
MT (visual area of superior temporal sulcus) in the marmoset (Callithrix jacchus)," Exp.
Brain Res., 27, 559-572, 1977.
4GB. Dow, "Functional classes of cells and their laminar distribution in monkey vi­
sual cortex," J. Neurophysiology, 37, 927-946, 1974; M. Livingstone and D. H. Hubel,
"Anatomy and physiology of a color system in the primate visual cortex," J. Neuro­
science, 4, 309-356, 1984; J. A. Movshon and W. T. Newsome, "Functional characteristics
of striate cortical neurons projecting to MT in the macaque," Soc. Neurosci. Abstr., 10,
933, 1984.
47S. Zeki, "Functional organization of a visual area in the posterior bank of the superior
MAPS IN CONTEXT: VISUAL CORTICAL AND GENETIC MAPS
381
highly sensitive to the direction of stimulus motion. Recently, Movshon and
collaborators 48 have found that some MT neurons respond to the appar­
ent direction of motion of complex' grating patterns, whereas V-I neurons
respond to the actual direction of motion of the components of the stimu­
lus, which can be quite different from the apparent direction of motion of
the whole pattern. Thus the properties of MT neurons more nearly match
perception and constitute a significant elaboration of function beyond that
found in V-I.
The parvocellular laminae project to layer 4CP in V_I,49 then to layers
two and three in V_I,5o then to sectors the second visual area (V-II),61 then
to the dorsolateral visual area (DL),52 then to inferotemporal cortex. This
temporal sulcus of the rhesus monkey," J. Physiology, 236, 549-573, 1974; J. F. Baker,
S. E. Petersen, W. T. Newsome and J. Allman, "Response properties in four extrastri­
ate visual areas of the owl monkey (Aotus triIJirgatus): a quantitative comparison of the
medial, dorsomedial, dorsolateral and middle temporal areas," J. Neurophysiology, 45,
397-416, 1981; J. H. R. Maunsell and D. Van Essen, "Functional properties of neurons in
middle temporal visual areas (MT) of macaque monkey. I. Selectivity for stimulus direc­
tion, velocity and orientation," J. Neurophysiology, 49, 1127-1167, 1983; T. D. Albright,
"Direction and orientation selectivity of neurons in visual area MT of the macaque," J.
Neurophysiology, 52, 1106-1130, 1984.
48J. A. Movshon, E. H. Adelson, M. S. Gizzi and W. T. Newsome, "The analysis of
moving visual patterns," in: Pattern recognition mechanisms, C. Chagas, R. Gattass and
C. Gross, eds., 117-151, Springer, New York, 1985; J. A. Movshon and W. T. Newsome,
"Functional characteristics of striate cortical neurons projection to MT in the macaque,"
Soc. Neurosci. Abstr., 10, 933, 1984.
9
4 D. H. Hubel and T. N. Wiesel, "Laminar and columnar distribution of genicula-cortical
fibers in the macaque monkey," J. Comparative Neurology, 146, 421-450, 1972.
50 J. Lund and R. Boothe, "Interlaminar connections and pyramidal neurons organization
in the visual cortex, area 17, of the macaque monkey," J. Comparative Neurology, 159,
305-334, 1975.
51 W. B. Spatz I J. Tigges and M. Tigges, "Subcortical projections, cortical associations
and some intrinsic interlaminar connections of the striate cortex in the squirrel monkey
(Saimin)," J. Comparative Neurology, 140, 155-173, 1970; M. Livingston and D. Hubel,
"Anatomy and physiology of a color system in the primate visual cortex," J. Neuroscience,
4, 309-356, 1984.
52R. E. Weller and J. H. Kaas, "Cortical projections of the dorsolateral visual area in owl
monkeys: the prestriate relay to inferior temporal cortex," J. Comparative Neurology, 234,
35-59, 1985. Area DL in New World Monkeys and prosimians probably corresponds to part
or all of the "V4 complex" in macaque monkeys. The V4 complex also receives input from
V-II. See S. Shipp and S. Zeki, "Segregation of pathways leading from area V2 to areas
V4 and V5 of macaque monkey visual cortex," Nature, 315, 322-325,1985; E. DeYoe and
382
JOHN ALLMAN
system appears to be devoted to the analysis of form and in some species to
color. DL neurons are highly selective to the size and shape of visual stimuli
irrespective of their exact position within their receptive fields. 53 Desimone
and collaborators54 have found striking evidence for shape selectivity for
neurons in inferotemporal cortex. Inferotemporal cortex is also strongly
implicated in the ability to learn to discriminate visual shapes. 55
Recently, evidence has emerged that there is a duplication of the map
within V-I in primates. 56 Stains for the activity of the mitochondrial en­
zyme, cytochrome oxidase, have revealed a regular, repeating pattern that
is unique to primates. 57 Livingstone and Hubel 58 have found that the neu­
rons in the cytochrome oxidase rich "blobs" lack orientation selectivity,
are rich in opponent-color mechanisms, and project to "thin stripes" of
high cytochrome oxidase activity in V-II. By contrast, they found that the
neurons in the "interblobs" in V-I are orientation selective and project to
stripes of low cytochrome oxidase activity in V-II. The thin stripes and the
interstripes project to the fourth visual area (V4).59 There are also "thick
stripes" of high cytochrome oxidase activity in V-II that project to MT.60
Thus, there are maps within maps in the first and second visual areas of priD. Van Essen, "Segregation of efferent connections and receptive field properties in visual
area V2 of the macaque," Nature, 317, 58-61, 1985. The V4 complex in turn projects
to infero-temporal cortex. See R. Desimone, J. Fleming and C. G. Gross, "Prestriate
afferents to inferior temporal cortex: an HRP study," Brain Res., 184, 41-55, 1980.
53S. E. Petersen, J. F. Baker and J. M. Allman, "Dimensional selectivity of neurons in
the dorsolateral visual area of the owl monkey," Brain Res., 197, 507-511, 1980.
54R. Desimone, T. Albright, C. G. Gross and C. Bruce, "Stimulus selective properties
of inferior temporal neurons in the macaque," J. Neuroscience, 4, 2051-2062, 1984.
5&C. G. Gross, "Inferotemporal cortex and vision," Prog. in Physiological Psychology,
5,77-115,1973.
56 I am indebted to Richard Andersen for suggesting this point of view to me.
57M. Wong-Riley first described the cytochrome-oxidase rich structure in primate visual
cortex; they have been studied extensively in a large number of primate species by J. C.
Horton in "Cytochrome oxidase patches: a new cytoarchitectonic feature of the monkey
visual cortex," Phil. Trans. Roy. Soc. Lond., 304, 199-253, 1984.
58M. Livingstone and D. Hubel, "Anatomy and physiology of a color system in the
primate visual cortex," J. Neurosci., 4, 309-356, 1984.
1)!lE. A. DeYoe and D. Van Essen, "Segregation of efferent connections and receptive
field propert.ies in visual area V2 of the macaque," Nature, 317,58-61, 1985; S. Shipp and
S. Zeki, "Segregation of pathways leading from area V2 to areas V4 and V5 of macaque
monkeys visual cortex," Nature, 315, 322-325, 1985. 60 ibid. ~
MAPS IN CONTEXT: VISUAL CORTICAL AND GENETIC MAPS
383
mate visual cortex, which may represent a gradual differentiation of maps
and related functions within a visual area.
There exists a good deal of evidence to support the notion that dif­
ferent visual field maps perform different functions in the visual system;
however there is also evidence that they share many visual response prop­
erties in common. 61 Molecular biology provides precedents for other pos­
sible functions of duplicated structure that may have some relevance to
our efforts to determine the functions of cortical maps. The tetrameric
hemoglobin molecule is more efficient in binding and releasing oxygen than
the monomeric myoglobin molecule, and thus, the function of the four
homologous chains of hemoglobin is to act cooperatively in this process,
rather than for each chain to have a separate and distinct function. 62 The
functions of the members of the vast family of immunoglobins are highly
overlapping. 63 These examples from molecular biology of cooperativity and
highly overlapping function of replicated structures provide some prece­
dence for similar distributions of function within the multiple cortical visual
areas.
16.5
Differentiation of replicated structures
Modern genetics has provided some insights as to how replicated structures
differentiate; in development. As Lewis 64 has put it:
"The segmentation pattern of the fly provides a model sys­
tem for studying how genes control development ... Flies almost
certairily evolved from insects with four wings instead of two,
and insects are believed to have corne from arthropod forms
with many legs instead of six. During the evolution of the fly,
two major groups of genes must have evolved: leg-suppressing
GIJ. F. Baker, S. E. Petersen, W. T. Newsome and J. M. Allman, opus cit., 1981.
G2V. M. Ingram, The Hemoglobins in Genetics and Evolution, Columbia University
Press, New York, 1963.
G3L. Hood, J. H. Campbell and S. C. R. Elgin, "The organization, expression and
evolution of antibody genes and other multigene families," Ann. Rev. Genetics, 9, 305­
353, 1975.
G4 E. B. Lewis, U A gene complex controlling segmentation in Drosophi/ia," Nature, 276,
565-570, 1978.
384
JOHN ALLMAN
genes which removed legs from abdominal segments of milliped­
like ancestors followed by haltere-promoting genes which sup­
pressed the second pair of wings of four-winged ancestors."
-J
In fruit flies, series of genes have been discovered that govern the forma­
tion of segments and their differentiation. These genes regulate the action of
other genes that cause each segment to differentiate. Lewis 65 has proposed
that these regulatory genes were the product of a series of gene duplica­
tions, and indeed the genes that control the differentiation of the posterior
thoracic and abdominal segments are located in an orderly series on the
third chromosome that corresponds to the order of differentiation of the
segments. 66 An anal~gous and possibly even homologous set of genes has
been discovered that governs the differentiation of the segments that con­
stitute the anterior thorax and head. 67 Each of these genes contains an 180
base pair sequence of DN A, called the "homeobox" that shows a high degree
of correspondence. The homeobox is also found in a large number of other
organisms including frogs, mice and humans. 68 The "homeobox" encodes
for a 60 amino acid long "homeo domain" that is rich in the basic amino
acids, lysine and arginine, which would enable the homeo domain to bind
to DNA.69 The homeo domain apparently has been strongly conserved in
evolution, possibly to perform the function of binding the regulatory gene
product to regulation sites in the DNA. Each regulatory gene may have
been the result of ancient gene replications, but only the correspondence in
this highly conserved portion is still easily identifiable. 70 Some of these reg­
ulatory genes for the fruit fly have been cloned. The in situ hybridization of
the cloned DNA is located primarily in the nervous system, where presum­
ably the genes regulate the differentiation of the neural circuitry for each
---
G&E. B. Lewis, "Pseudoallelism and gene evolution," Cold Spring Harbor Symposia in
Quantitative Biology, 16, 159-174, 1951.
GGE. B. Lewis, opus cit., 1978.
G7W. J. Gehring, "The molecular basis of development," Scientific American, October,
1985, pp. 153-162.
G8 ibid.
Gf) A. Laughton and M. P. Scott, "Sequence of a Drosophilia segmentation gene: protein
structure homology with DNA-binding proteins," Nature, 310, 25-31, 1984.
70 Alternatively, these highly conserved sequences could be the product of convergent
evolution.
MAPS IN CONTEXT: VISUAL CORTICAL AN D GENETIC MAPS
385
segment,ll In mammals, an analogous set of genes could regulate the seg­
mentation of the cerebral cortex into distinct areas, and the differentiation
the neural circuitry in each area.
16.6
The influence of context
Gene expression is the integrated.product of a host of influences arising from
the action of regulatory genes, circulating hormones and many other factors
that comprise the context. Similarly, the visual responses of neurons within
a visuotopic map in a cortical area are likely to be the product of a broad
array of contextual influences. However, it has typically been assumed that
neurons at any particular locus within a map are not influenced by visual
stimuli presented outside their receptive fields. Further, it has been widely
assumed that perceptual functions that require the integration of inputs
over large portions of the visual field must be either collective properties of
arrays of neurons representing the visual field, or features of those neurons
at the highest processing levels in the visual system, such as the cells in
inferotemporal or posterior parietal cortex that typically possess very large
receptive fields and do not appear to be organized in visuotopic maps.12
These assumptions have been based on the results of the many studies in
which receptive fields were mapped with conventional stimuli, presented
one at a time, against a featureless background. This has been termed
the classical receptive field or CRF. 73 However, unlike the neurophysiolo­
gist's tangent screen, the natural visual scene is rich in features, and there
is a growing body of evidence that in many visual neurons, stimuli pre­
sented outside the eRF strongly and selectively influence neural responses
to stimuli presented within the CRF. For example, Miezin, McGuiness and
174 found that the direction and velocity of stimuli presented outside the
7I M. P. Scott, "Homeotic gene transcripts in the neural tissue of insects," Trends in
Neurosciences, '1, 221-223, 1984.
72 J. Allman, F. Miezin and E. McGuinness, "Stimulus specific responses from beyond
the classical receptive field: neurophysiological mechanisms for local-global comparisons
in visual neurons," Ann. Rev. Neurosci., 8, 407-430, 1985.
73ibid.
74 ibid.; J. Allman, F. Miezin and E. McGuinness, "Direction and velocity specific re­
sponses from beyond the classical receptive field in cortical visual area MT," Perception,
4, 105-126, 1985.
~
386
JOHN ALLMAN
CRF for MT neurons strongly and selectively influenced the responses of
the stimuli presented simultaneously within the CRF. (See Figure 16.4.) By
selectively masking off various regions of the visual field outside the CRF,
we mapped the total receptive field (TRF) for these neurons, which turned
out to be 50 to 100 times the area of the CRF's or virtually the whole
visual field in some cases. About 90% of MT neurons possess these large
surrounds, which can only be detected by measuring the influence of stim­
uli presented there on the responses to stimuli presented within the CRF.
We also have found similar, but less extensive, surround effects beyond the
CRF for neurons in V-I and V-II. Similar effect.s have been reported in the
optic tectum in pigeons 75 and in visual cortex in cats. 76 Recent recordings
from neurons in the V4 complex in macaque monkeys have revealed broad
surround regions tuned for orientation, spatial frequency and color. 77 The
TRF's provide mechanisms that may serve as the basis for many functions
in vision, such as the perceptual constancies, figure-ground discrimination,
and depth perception through motion.
As mentioned above, some MT neurons lack the surround. We have
. recorded adjacent neurons that had the same CRF and direction preference,
one neuron with and one neuron without an antagonistic surround. By
comparing the responses of these two neurons, it would be possible for a
higher order neuron to infer whether a particular movement had been a local
movement restricted to a small part of the .visual field or part of a larger
pattern of movement in the same direction,'which might have been due to
movement by the animal itself. Such computations could contribute to the
organism's solution of the "stability of the visual world problem" through
visual input alone, as has been suggested by Gibson 78 and Koenderink. 79
75 J. 1. Nelson and B. Frost, "Orientation selective inhibition from beyond the dassic
visual receptive field," Brain Res., 139, 359-365, 1978; P. L. Scilley, S. C. P. Wong,
"Moving background patterns reveal double-opponency of directionally specific pigeon
tectal neurons," Exp. Brain Res., 43, 173-185, 1981.
7GM. Von Grunau and B. J. Frost, "Double-opponent-process mechanism underlying
RF-structure of directionally specific cells of cat lateral suprasylvanian visual area," Exp.
Brain Res., 49, 84-92, 1983.
77R. Desimone, S. Schien, J. Moran and L. Ungerleider, "Contour, color and shape
analysis beyond the striate cortex," Vis. Res., 25, 441-452, 1985.
7S J. J. Gibson, The Senses Considered as Perceptual Systems, Houghton Mifflin, Boston,
1966.
79 J. J. Koenderink, "Space, form and optical deformation," in: Brain Mechanisms and
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388
JOHN ALLMAN
Visual cortex neurons have been demonstrated to have the potential
to make other types of inferences on the basis of responses to stimuli pre­
sented beyond the CRF. Von der Heydt and collaborators 80 discovered that
about one third of the neurons in the second visual area in awake macaque
monkeys respond to illusory contours when the real contours evoking the
response were located entirely outside the CRF. The perception of illu­
sory contours might be considered as a type of constancy, since the visual
system is interpolating a continuous contour from an interrupted contour,
which under natural conditions would be produced by a partially occlud­
ing surface. The tropical forest environment, in which primates evolved,
abounds with occluding foliage and branches, and the ability to reconstruct
surfaces that are partially hidden from view would be very adaptive. Sim­
ilarly, Zeki81 has recorded neurons in the V4 complex that exhibit color
constancy, that is they respond to the apparent color of the stimulus re­
gardless of the spectral content of the stimulus. Again, the ability to make
such inferences would have been of great adaptive value to our primate
forebearers since it would have enabled t.hem, for example, to identify ripe
fruit, suitable to eat, on the basis of their colors under a broad range of
different environmental lighting conditions. In each case, the neuron ap­
pears' to be making inferences about what is happening within its CRF on
the basis of stimuli occurring elsewhere in the visual field. This process
{or making inferences on the basis of comparisons between local and more
global stimqli may have served as the base upon which other cognitive ca­
pacities for logical inference developed in the evolution of other cortical
areas.
What is the anatomical basis in fiber connections for the extensive sur­
rounds of visual cortical neurons? The ascending connections closely match
the visuotopic organization of the CRF's.82 Intrinsic connections within
each visuotopic map probably contribute to some extent to the surrounds,
Spatial Vision, D. Ingle, D. Lee and M. Jeannerod, eds., Nijhot, The Hague, 1984.
811R. Von der Heydt, E. Peterhand" and C. Baumgartner, "Illusory contours and cortical
neuron responses," Science, 224, 1260-1262, 1984.
8! S. M. Zeki, "Color coding in the cerebral cortex: the responses of wavelength-selective
and color-coded cells in monkey visual cortex to changes in wavelength composition,"
Neuroscience, 9, 767-781, 1983.
82R. E. Weller and J. J. Kaas, "Retinotopic patterns of connections of area 17 with
visual areas V-II and MT in macaque monkeys," J. Comparative Neurology, 228, 81-104,
1983.
MAPS IN CONTEXT: VISUAL CORTICAL AND GENETIC MAPS
389
but the main source of input to the surrounds probably comes from struc­
tures higher in the system. 83 Ascending projections terminate in layer 4
of each cortical area, while descending projections terminate in the other
layers, particularly in layers 1 and 6. 84 It is particularly interesting that one
cortical area, the medial (M), which has a map which emphasizes the more
peripheral parts of the visual field, has no ascending outputs according
to its laminar connections; it only feeds back upon other cortical areas. 8S
Thus, the function of area M and perhaps some of the other extrastriate
areas may be largely to provide feedback for the elaboration of surround
mechanisms in other areas. They would thus have functions analogous to
regulatory genes or controlling elements in genetics. 86
Recent investigations have also demonstrated important attentional and
non-visual inputs to visuotopically mapped cortical areas. For example,
Moran and Desimone87 have found in trained monkeys that the spatial lo­
cation of focal attention gates visual processing by filtering out irrelevant
visual information within the classical receptive fields of neurons in V4 and
IT. Maunsell and Haenny88 have trained monkeys to match the orienta­
tion of a visually presented grating with a tactually presented grating and
recorded the responses of V4 neurons during this task. Sixty percent of the
V4 cells were influenced by the orientation of the tactile grating which was
not visible to the monkey; some of these responses were very specific and
are likely to have developed as a consequence of the animal's training. It
is not clear how these influences are relayed to the visuotopically mapped
areas; however, one very interesting set of connections has recently been
demonstrated between the amygdala, which is strongly implicated in mem­
ory processes,89 and· the visual c~rtex. The inferotemporal visual cortex
83 J.
Allman, F. Miezin, E. McGuinness," opus cit., 1985.
84J. H. R. Maunsell and D. C. Van Essen, "The connections of the middle temporal
visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey,"
J. Neuroscience, 3, 2563-2586, 1983.
85 J. Graham, J. Wall and J. Kaas, "Cortical projections of the medial visual area in the
owl monkey, Aotus trivirgatus," Neuroscience Letters, 15, 109-114, 1979.
8GB. McClintock, "Controlling elements and the gene," Cold Spring Harbor Symposia in
Quantitative Biology, 21, 197-216, 1956.
87 J. Moran and R. Desimone, "Selective attention gates visual processing in the extras­
triate cortex," Science, 229, 782-784, 1985.
88 J. H. R. Maunsell, penonal communication.
8DM. Mishkin, "A memory system in the monkey," Phil. Trans. of the Roy. Soc. B,
390
.. JOHN ALLMAN
projects upon portions of the amygdala in an ascending fashion; the amyg­
dala nuclei are extensively interconnected, and other parts of the amygdala
are reciprocally interconnected with the neuroendocrine centers of the hy­
pothalamus. Recently Amaral and Price90 have demonstrated that the
amygdala projects to the junction between layers 1 and 2 in many of the
cortical visual areas in macaque monkeys. This provides an avenue for in­
fluences from systems involved in memory and neuroendocrine functions to
mediate responses within the visuotopically mapped cortical areas.
The function of the visual system is not merely to create a precise
neural analogue of the optic image on the photoreceptors, but beyond this,
to reconstruct behaviorally significant features of the visual environment
on the basis of imperfect and unconstant information. Neurons in cortical
maps appear to make inferences about attributes of the visual world on
the basis of local-global comparisons in the visual field, while taking into
account the organism's past experience and attentional state.
Finally, I would like to return to the original theme of this essay and
make one last comparison between molecular genetics and the neurobiol­
ogy of visual cortex. Molecular geneticists have discovered a great deal
about the organization and action of specific genes, but, apart from some
promising leads, they have not yet discovered how even simple organs are
put together from the genetic instructions. Similarly, those of us who study
the visual cortex have been able to learn a great deal abo.ut its anatomical
organization and the properties of individual neurons witbin it, but again,
apart from some promising leads, we have not yet discovered how these are
put together to form percepts or thoughts. I would like to suggest that
the molecular genetics of organ assembly and the neurobiology of percep­
tion and cognition will each provide a rich source of analogies to stimulate
exploration in the other field.
Acknowledgement: This work was supported by NIH grant EY-03851.
[John Allman, Ph.D., is a member of the Beckman Laboratory, Division of
Biology, California Institute of Technology, Pasadena, Caltforr.;a 91125.]
298, 85-96, 1982.
DOD. G. Amaral and J. L. Price, "Amygdalo-cortical projections in the monkey (Macaca
jascicularis)," J. Comparative Neurology, 2S0, 465-496, 1984.
392
JOHN ALLMAN
owl monkey (Aotus trivirgatus)," Brain Res., 35,89-106,1971; "The orga­
nization of the second visual area (V-II) in the owl monkey: a second order
transformation of the visual hemifield," Brain Res., 76,247-265,1974; "A
crescent-shaped cortical area surrounding the middle temporal area (MT)
in the owl monkey (Aotus trivirgatus)," Brain Res., 81, 199-213,1974; "The
dorsomedial cortical visual area: a third tier area in the occipital lobe of
the owl monkey (Aotus trivirgatus)," Brain Res., 100,473-487, 1975; "Rep­
resentation of the visual field on the medial wall of the occipital-parietal
cortex of the owl monkey (Aotus trivirgatus)," Science, 191,572-575,1976;
W. T. Newsome and J. Allman, "The interhemispheric connections of vi­
sual cortex in the owl monkey, Aotus trivirgatus, and th"e bushbaby, Galago
senegalensis," J. Compo Neurol., 194, 209-234, 1980]. The somatosensory
areas were mapped by M. Merzenich, J. Kaas, M. Sur and .C. S. Lin ["Dou­
ble representation of the body surface within cytoarchitectonic areas 3b and
1 in the owl monkey (Aotus trivirgatus)," J. Compo Neurol., 181, 41-74,
1978]. The auditory areas were mapped by T. J. Imig, M. A. Ruggero, L.
M. Kitzes, E. Javel and J. Brugge ["Organization of auditory cortex in the
owl monkey (Aotus trivirgatus)," J. Compo Neurol., 171, 111-128, 1977].
The subdivisions of superior temporal and inferotemporal visual cortex are
based on the connectional s~udies of R. Weller [Subdivisions and connec­
tions of inferior temporal cortex in owl monkeys, Doctoral Dissertation,
Vanderbilt University, Nashville, Tennessee].
Figure 16.3: Left: dorsal view of the skull of Tetonius homunculus.
A.M.N.H. No. 4194. Right: dorsal view of Radinsky's reconstruction of
the cranial endocast of Tetonju~. OB: olfactory bulb. S: sylvian sulcus.
Reproduced from L. B. Radinsky, "Oldest primate endocast," American J.
Phys. Anthropology, 27, 385-388, 1967. Courtesy of Wistar Press. Note
the large expansion of occipital-temporal cortex in Tetonius. Many of the
areas illustrated in Figure 16.2, including V-I, V-iii DL, MT, M and ITc
were probably present in the early primates of the Eocene such as Tetonius
because they are present in modern galagos, whose most recent common
ancestor with monkeys would have lived no more recently than the early
Eocene. [J. Allman, J. Kaas and R. Lane, "The middle temporal visual
area (MT) in the bushbaby, Galago senegalensis," Brain Res., 40, 197-202,
1973; J. Allman, C. B. G. Campbell and E. McGuinness, "The dorsal third
tier area in Galago senega((insis," Brain Res., 179,355-361,1979; J. Allman
-
MAPS IN CONTEXT: VISUAL CORTICAL AND GENETIC MAPS
393
and E. McGuinness, unpublished mapped data for Galago senegalensis.]
Figure 16.4: Direction-selective- neuron with an antagonistic direction­
selective surround recorded from the middle temporal visual area (MT)
in the owl monkey. The left graph depicts the response of the cell to 12
directions of movement of an array of random dots within an area coexten­
sive with its CRF. The response is normalized so that 0% is equal to the
average level of spontaneous activity sampled for 2-second periods before
each presentation. Negative percentages in the left graph indicate inhibi­
tion relative to the level of spontaneous activity. In the left graph, the­
response to the. optimum direction is 100%. The right graph depicts the
response of the cell to different direction of background movement, while
the CRF was simultaneously stimulated by the array of dots moving in the
cells preferred direction. The stimulus conditions are depicted schemati­
cally above each graph. In the experiment, the dots were 50% dark, 50%
light, and the background was much larger relative to the center than is
depicted schematically. Reproduced from: J. Allman, F. M. Miezin and
E. McGuinness, "Stimulus selective responses from beyond the classical re­
ceptive field," Ann. Rev. Neuro., 8, 407-430, 1985. Courtesy of Annual
Review, Inc.